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Neurospora tetrasperma from Natural Populations: Toward the Population Genomics of a Model Fungus
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
2013 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The study of DNA sequence variation is a powerful approach to study genome evolution, and to reconstruct evolutionary histories of species. In this thesis, I have studied genetic variation in the fungus Neurospora tetrasperma and other closely related Neurospora species. I have focused on N. tetrasperma in my research because it has large regions of suppressed recombination on its mating-type chromosomes, had undergone a recent change in reproductive mode and is composed of multiple reproductively isolated lineages. Using DNA sequence data from a large sample set representing multiple species of Neurospora I estimated that N. tetrasperma evolved ~1 million years ago and that it is composed of at least 10 lineages. My analysis of the type of asexual spores produced using newly described N. tetrasperma populations in Britain revealed that lineages differ considerably in life history characteristics that may have consequences for their evolution. A comparative genomic analysis using three genomes of N. tetrasperma and the genome of N. crassa revealed that the mat a chromosomes in the lineages examine have been introgressed from other Neurospora species and that this introgression has reduced levels of molecular degeneration on the mating-type chromosomes. Finally, I generated a population genomic dataset composed of 92 N. tetrasperma genomes and two genomes of other Neurospora species. Analysis of these genomes revealed that all strains of N. tetrasperma have large regions of suppressed recombination on their mating-type chromosomes ranging from 69-84% of the chromosome and that the extent of divergence between mating-type chromosomes within lineages varies greatly (from 1.3 to 3.2%). I concluded that the source of this great divergence mating-type chromosome is large-scale introgression from other Neurospora species, and that these introgressed tracts have become fixed within N. tetrasperma lineages. I also discovered that genes within non-recombining introgressed regions of the mating-type chromosome have severely reduced levels of genetic variation as compared to the autosomes, and exhibit signatures of reduced molecular degeneration. My analysis of variation in coding regions revealed that positive selection on the introgressed regions has resulted in the removal of deleterious mutations and is responsible for the reductions in molecular degeneration observed.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2013. , 52 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1084
Keyword [en]
Neurospora, poulation genetics, genomes, introgression
National Category
Evolutionary Biology Genetics
Research subject
Evolutionary Genetics
Identifiers
URN: urn:nbn:se:uu:diva-208791ISBN: 978-91-554-8771-3 (print)OAI: oai:DiVA.org:uu-208791DiVA: diva2:654771
Public defence
2013-11-22, Zootisalen, EBC, Uppsala, 09:00 (English)
Opponent
Supervisors
Available from: 2013-10-31 Created: 2013-10-07 Last updated: 2014-01-23
List of papers
1. Large-Scale Introgression Shapes the Evolution of the Mating-Type Chromosomes of the Filamentous Ascomycete Neurospora tetrasperma
Open this publication in new window or tab >>Large-Scale Introgression Shapes the Evolution of the Mating-Type Chromosomes of the Filamentous Ascomycete Neurospora tetrasperma
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2012 (English)In: PLOS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 8, no 7, e1002820- p.Article in journal (Refereed) Published
Abstract [en]

The significance of introgression as an evolutionary force shaping natural populations is well established, especially in animal and plant systems. However, the abundance and size of introgression tracts, and to what degree interspecific gene flow is the result of adaptive processes, are largely unknown. In this study, we present medium coverage genomic data from species of the filamentous ascomycete Neurospora, and we use comparative genomics to investigate the introgression landscape at the genomic level in this model genus. We revealed one large introgression tract in each of the three investigated phylogenetic lineages of Neurospora tetrasperma (sizes of 5.6 Mbp, 5.2 Mbp, and 4.1 Mbp, respectively). The tract is located on the chromosome containing the locus conferring sexual identity, the mating-type (mat) chromosome. The region of introgression is confined to the region of suppressed recombination and is found on one of the two mat chromosomes (mat a). We used Bayesian concordance analyses to exclude incomplete lineage sorting as the cause for the observed pattern, and multilocus genealogies from additional species of Neurospora show that the introgression likely originates from two closely related, freely recombining, heterothallic species (N. hispaniola and N. crassa/N. perkinsii). Finally, we investigated patterns of molecular evolution of the mat chromosome in Neurospora, and we show that introgression is correlated with reduced level of molecular degeneration, consistent with a shorter time of recombination suppression. The chromosome specific (mat) and allele specific (mat a) introgression reported herein comprise the largest introgression tracts reported to date from natural populations. Furthermore, our data contradicts theoretical predictions that introgression should be less likely on sex-determining chromosomes. Taken together, the data presented herein advance our general understanding of introgression as a force shaping eukaryotic genomes.

National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-181143 (URN)10.1371/journal.pgen.1002820 (DOI)000306840400034 ()
Available from: 2012-09-18 Created: 2012-09-17 Last updated: 2017-12-07Bibliographically approved
2. Quantifying functional heterothallism in the pseudohomothallic ascomycete Neurospora tetrasperma
Open this publication in new window or tab >>Quantifying functional heterothallism in the pseudohomothallic ascomycete Neurospora tetrasperma
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2012 (English)In: Fungal Biology, ISSN 1878-6146, E-ISSN 1878-6162, Vol. 116, no 9, 962-975 p.Article in journal (Refereed) Published
Abstract [en]

Neurospora tetrasperma is a pseudohomothallic filamentous ascomycete that has evolved from heterothallic ancestors. Throughout its life cycle, it is predominantly heterokaryotic for mating type, and thereby self-fertile. However, studies of N. tetrasperma have revealed the occasional production of self-sterile asexual and sexual spores of a single-mating type, indicating that it can be functionally heterothallic. Here, we report the extensive sampling and isolation of natural, heterokaryotic, strains of N. tetrasperma from the United Kingdom (UK): 99 strains were collected from Surrey, England, and four from Edinburgh, Scotland. We verified by phylogenetic analyses that these strains belong to N. tetrasperma. We isolated cultures from single germinated asexual spores (conidia) from 17 of these newly sampled UK strains from Surrey, and 16 previously sampled strains of N. tetrasperma from New Zealand (NZ). Our results show that the N. tetrasperrna strains from the UK population produced a significantly greater proportion of self-sterile, homokaryotic conidia than the NZ population: the proportion of homokaryotic conidia was 42.6 % (133/312 spores) and 15.3 % (59/386) from the UK and the NZ populations, respectively. Although homokaryons recovered from several strains show a bias for one of the mating types, the total ratio of mat A to mat a mating type in homokaryons (UK: 72/61, NZ 28/31) did not deviate significantly from the expected 1:1 ratio for either of these populations. These results indicate that different populations exhibit differences in their life cycle characteristics, and that a higher degree of outcrossing might be expected from the UK population. This study points to the importance of studying multiple strains and populations when investigating life history traits of an organism with a complex life cycle, as previously undetected differences between populations may be revealed.

Keyword
Conidia, Heterothallism, Neurospora tetrasperma, Outcrossing, Populations, Pseudohomothallism
National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-185648 (URN)10.1016/j.funbio.2012.06.006 (DOI)000310038800003 ()
Available from: 2012-11-27 Created: 2012-11-27 Last updated: 2017-12-07Bibliographically approved
3. A global multilocus analysis of the model fungus Neurospora reveals a single recent origin of a novel genetic system
Open this publication in new window or tab >>A global multilocus analysis of the model fungus Neurospora reveals a single recent origin of a novel genetic system
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2014 (English)In: Molecular Phylogenetics and Evolution, ISSN 1055-7903, E-ISSN 1095-9513, Vol. 78, 136-147 p.Article in journal (Refereed) Published
Abstract [en]

The large diversity of mating systems observed in the fungal kingdom underlines the importance of mating system change in fungal evolution. The selfing species Neurospora tetrasperma has evolved a novel method of achieving self-fertility by a mating system referred to as pseudohomothallism. However, little is known about the origin of N. tetrasperma and its relationship to the self-sterile, heterothallic, Neurospora species. In this study, we used a combination of phylogenetic and population genetic analyses to reconstruct the evolutionary history of N. tetrasperma and its heterothallic relatives. We sequenced 9 unlinked nuclear loci from 106 strains of N. tetrasperma sampled from across the globe, and a sample of 28 heterothallic strains of Neurospora. Our analyses provide strong support for monophyly of N. tetrasperma, but reject the monophyly of N. crassa. We estimate that N. tetrasperma is of a recent origin and that it diverged from the heterothallic species ~1 million years ago. We also extend previous findings on the diversification within the N. tetrasperma clade, with 10 lineages identified. Taken together, these findings indicate that N. tetrasperma is younger than has been previously reported and that a rapid diversification of lineages has occurred within the N. tetrasperma clade.

Keyword
Mating Systems, Population Structure, Phylogenetics, Neurospora
National Category
Evolutionary Biology
Research subject
Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-208792 (URN)10.1016/j.ympev.2014.05.007 (DOI)000342480400012 ()
Available from: 2013-10-07 Created: 2013-10-07 Last updated: 2017-12-06Bibliographically approved
4. Adaptive introgression slows down molecular degeneration of the mating-type chromosome in Neurospora tetrasperma
Open this publication in new window or tab >>Adaptive introgression slows down molecular degeneration of the mating-type chromosome in Neurospora tetrasperma
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(English)Manuscript (preprint) (Other academic)
Keyword
Neurospora, introgression, recombination, genomes
National Category
Evolutionary Biology Genetics
Research subject
Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-208794 (URN)
Available from: 2013-10-07 Created: 2013-10-07 Last updated: 2014-01-23

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